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Genetic Diversity, Ochratoxin a and Fumonisin Profiles of Strains of Aspergillus Section Nigri Isolated from Dried Vine Fruits

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Genetic Diversity, Ochratoxin a and Fumonisin Profiles of Strains of Aspergillus Section Nigri Isolated from Dried Vine Fruits toxins Article Genetic Diversity, Ochratoxin A and Fumonisin Profiles of Strains of Aspergillus Section Nigri Isolated from Dried Vine Fruits Petra Mikušová 1,* , Miroslav Cabo ˇn 1, Andrea Melichárková 1 , Martin Urík 2, Alberto Ritieni 3 and Marek Slovák 1,4 1 Plant Science and Biodiversity Centre, Institute of Botany, Slovak Academy of Sciences, Dúbravská cesta 9, SK-845 23 Bratislava, Slovakia; [email protected] (M.C.); [email protected] (A.M.); [email protected] (M.S.) 2 Institute of Laboratory Research on Geomaterials, Faculty of Natural Sciences, Comenius University in Bratislava, Ilkoviˇcova6, SK-842 15 Bratislava 4, Slovakia; [email protected] 3 Department of Pharmacy, School of Medicine, University of Naples Federico II, Staff of Unesco Chair for Health Education and Sustainable Development, 801 31 Napoli, Italy; [email protected] 4 Department of Botany, Charles University, Benátská 2, CZ-128 01 Praha 2, Czech Republic * Correspondence: [email protected] Received: 23 July 2020; Accepted: 9 September 2020; Published: 14 September 2020 Abstract: We investigated ochratoxin A (OTA) contamination in raisin samples purchased from Slovak markets and determined the diversity of black-spored aspergilli as potential OTA and fumonisin (FB1 and FB2) producers. The taxonomic identification was performed using sequences of the nuclear ITS1-5.8s-ITS2 region, the calmodulin and beta-tubulin genes. We obtained 239 isolates from eight fungal genera, of which 197 belonged to Aspergillus (82%) and 42 strains (18%) to other fungal genera. OTA contamination was evidenced in 75% of the samples and its level ranged from 0.8 to 10.6 µg/kg. The combination of all three markers used enabled unambiguous identification of A. carbonarius, A. luchuensis, A. niger, A. tubingensis and A. welwitschiae. The dominant coloniser, simultaneously having the highest within-species diversity isolated from our raisin samples, was A. tubingensis. Out of all analysed strains, only A. carbonarius was found to produce OTA, but in relatively high quantity (2477–4382 µg/kg). The production of FB1 and FB2 was evidenced in A. niger strains only. Keywords: food spoilage; mycotoxin; fungal diversity; calmodulin; beta-tubulin; HPLC Key Contribution: The incidence of five species from Aspergillus section Nigri (A. carbonarius; A. luchuensis; A. niger; A. welwitschiae; A. tubingensis) was detected on analysed raisin samples. The most prevalent species with the highest genetic diversity was A. tubingensis. The maximum tolerable value of OTA reaching a critical threshold of 10 µg/kg was exceeded only in two samples out of the 20 analysed. The ochratoxigenic ability was confirmed only in A. carbonarius strains, while FB1 and FB2 production was found in isolates of A. niger. 1. Introduction Dried vine fruits are some of the most favourite and frequently utilised ingredients in the food industry; however, they are often exposed to contamination by metabolites of various microorganisms, including filamentous fungi [1]. The fungal genus Aspergillus comprises numerous species which significantly impact overall food production and human health [2]. Out of them, members of the Aspergillus section Nigri [3] are considered to be some of the most influential food contaminants of dried vine fruit products worldwide. These microorganisms are well known as important producers Toxins 2020, 12, 592; doi:10.3390/toxins12090592 www.mdpi.com/journal/toxins Toxins 2020, 12, 592 2 of 15 of a large scale of mycotoxins, but especially ochratoxins and fumonisins [4]. Indeed, members of the Aspergillus section Nigri were proven to be the main OTA (ochratoxin A) producers in grapes and are responsible for the contamination of wine, grape juice and raisins [5–8]. OTA is one of the most harmful and most strictly monitored mycotoxins [9,10]. The European Commission determined the maximum OTA limit for raisins at 10 µg/kg [11]. The accurate number of black aspergilli species producing OTA is still enigmatic because of uncertainty in their identification [2,12]. Likewise, fumonisins also belong to toxic secondary metabolites produced by members of black aspergilli species and can be considered a possible source of mycotoxin contamination. The classification of fumonisins is based on their structure, resulting in four classification groups—namely A, B, C and P. The most frequent and abundant in food commodities are, however, only FB1, FB2 and FB3 [13,14]. Importantly, FB1 and FB2 were found to be potentially carcinogenetic, and their presence in food was associated with a high incidence of human oesophageal cancer in China and South Africa [15,16]. The fumonisins were evidenced to be produced predominantly by specific members of the genus Fusarium (e.g., [4,13]). Nevertheless, their production has also been evidenced in some members of the Aspergillus species, specifically in A. niger, and rarely also in A. welwitschiae, to date [17–20]. Correct determination of the members of Aspergillus section Nigri has also been challenging for specialists in the taxonomy and evolution of the genus Aspergillus [21,22]. The taxonomy of this species group has been intensively studied by many taxonomists, and the most current taxonomic concept of black aspergilli recognises 27 well-delimited species [2,23–25]. The pivotal problem hampering unambiguous delimitation of black aspergilli is embodied in their cryptic speciation. Due to the lack of taxonomically diagnostic features, black aspergilli are hardly distinguishable by traditional micro- and macromorphological approaches [2,26,27]. Various DNA fingerprinting methods [28,29] and/or utilisation of low-copy protein-coding genes were shown to be the most efficient tools for reliable identification of species from the Aspergillus section Nigri [2,8,27]. In the present study, we investigated OTA contamination of dried vine fruit packages of various origins purchased in Slovak markets and analysed the taxonomic diversity and the ochratoxin and fumonisin (FB1 and FB2) production ability of the black aspergilli strains isolated. The following questions were addressed: (1) What is the level of OTA in the analysed dried vine fruit samples, and does the OTA content exceed the critical maximum limit of 10 µg/kg? (2) What is the overall diversity of microscopic fungi colonising the dried vine fruit samples? How many species from the Aspergillus section Nigri can be isolated and identified in the tested samples? (3) What are the individual ochratoxigenic abilities of selected isolated strains of members of Aspergillus section Nigri? Do some isolated black aspergilli strains produce fumonisins FB1 and FB2? 2. Results 2.1. Cultivations and Morphological Identifications The initial screening of the analysed dried vine fruit samples revealed that, except two samples, all were colonised by microfungi. The level of contamination ranged between 2.7 102 × and 3.6 103 CFU/g. The direct plating method onto malt extract agar (MEA) agar recovered × 239 isolates, representing 14 taxa and belonging to 8 genera of Alternaria, Cladosporium, Aspergillus, Paecilomyces, Penicillium, Rhizopus, Saccharomyces and Trichothecium (Table1). Based on the macro- and micromorphological identifications, only the strains of Alternaria alternata, Cladosporium cladosporioides, Penicillium chrysogenum and Trichothecium roseum were identified unambiguously at the species level. Toxins 2020, 12, 592 3 of 15 Table 1. Details on the origins of the analysed dried vine fruit samples, their taxonomic affiliation and codes of isolated fungal strains and OTA content detected. Abbreviations: RSA = Republic of South Africa; b.d.l. = below the detection limit. Level of Colony Occurrence of Sample Country of OTA Forming Units Aspergillus Strain Another Fungal ID Origin Aspergillus spp. Sect. Nigri Code Taxa Isolated (µg/kg) (CFU)/g within CFU A. niger G_209 Penicillium sp. G_45 Rhizopus sp. DVF_01/2016 Chile b.d.l. 2.2 103 84% × A. tubingensis G_178 G_211 G_180 - DVF_02/2016 Iran b.d.l. 5.4 102 100% A. tubingensis × G_182 A. niger G_33 Aspergillus flavus DVF_03/2016 Iran 1.7 2.2 103 88% × A. welwitschiae G_36 Rhizopus sp. G_202 A. luchuensis G_201 DVF_04/2016 Chile 1.6 9 102 80% Rhizopus sp. × G_204 A. tubingensis G_203 Cladosporium G_198 Czech A. luchuensis cladosporioides DVF_05/2016 1.6 1.4 103 88% Republic × G_199 Penicillium sp. A. welwitschiae G_196 Slovak A. luchuensis G_62 DVF_06/2016 b.d.l. 9.9 102 100% - Republic × A. niger G_50 Penicillium sp. DVF_07/2016 Turkey b.d.l. 1.1 103 77% A. tubingensis G_132 Rhizopus sp. × Saccharomyces sp. Aspergillus flavus Cladosporium DVF_08/2016 Turkey 1.6 2.7 102 0% - - × cladosporioides Trichothecium roseum Alternaria alternata Paecilomyces sp. DVF_09/2016 Chile 10.5 6.3 102 14% A. tubingensis G_160 × Penicillium chrysogenum Saccharomyces sp. Rhizopus sp. DVF_10/2016 Chile 1.8 1.2 103 42% A. welwitschiae G_166 × Saccharomyces sp. DVF_11/2016 unknown 0.8 0 0% - -- DVF_12/2016 Iran 1.8 3.6 103 10% A. tubingensis G_168 - × G_171 Penicillium sp. DVF_13/2016 Chile 10.6 4.5 102 40% A. tubingensis × G_172 Saccharomyces sp. G_183 DVF_14/2016 RSA 2.5 6.2 102 71% A. tubingensis Saccharomyces sp. × G_184 A. carbonarius G_187 DVF_15/2016 Iran 1.2 1.9 103 91% Rhizopus sp. × A. tubingensis G_188 A. carbonarius G_191 DVF_16/2016 Turkey 1.8 1.9 103 91% G_190 Rhizopus sp. × A. tubingensis G_192 Czech DVF_17/2016 b.d.l. 0 0% - -- Republic DVF_18/2016 Uzbekistan 2.1 1.1 103 100% A. tubingensis G_174 - × A. niger G_210 DVF_19/2016 Chile 3.9 9.9 102 100% - × A. tubingensis G_61 DVF_20/2016 unknown 1.3 4.5 12 100% A. tubingensis G_176 - × Strains in bold were selected for individual analyses for toxigenic ability using HPLC (see Methods). Toxins 2020, 12, 592 4 of 15 The predominating colonisers, found in 90% of the samples, belonged to the genus Aspergillus. Out of the 239 isolated strains, 197 represented the genus Aspergillus (82%), while only 42 strains (18%) were assigned to other fungal genera. The percentage of aspergilli in the CFUs (colony forming units) oscillated was between 0 and 100%.
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